Tradeoffs between phage resistance and nitrogen fixation drive the evolution of genes essential for cyanobacterial heterocyst functionality.

Publisher: Oxford University Press Country of Publication: England NLM ID: 101301086 Publication Model: Print Cited Medium: Internet ISSN: 1751-7370 (Electronic) Linking ISSN: 17517362 NLM ISO Abbreviation: ISME J Subsets: MEDLINE

Publication: 2024- : Oxford : Oxford University Press
Original Publication: London : Nature Pub. Group

Bacteriophages*/genetics ; Nostoc*/genetics; Nitrogen Fixation/genetics ; Phylogeny ; Nitrogen

Harmful blooms caused by diazotrophic (nitrogen-fixing) Cyanobacteria are becoming increasingly frequent and negatively impact aquatic environments worldwide. Cyanophages (viruses infecting Cyanobacteria) can potentially regulate cyanobacterial blooms, yet Cyanobacteria can rapidly acquire mutations that provide protection against phage infection. Here, we provide novel insights into cyanophage:Cyanobacteria interactions by characterizing the resistance to phages in two species of diazotrophic Cyanobacteria: Nostoc sp. and Cylindrospermopsis raciborskii. Our results demonstrate that phage resistance is associated with a fitness tradeoff by which resistant Cyanobacteria have reduced ability to fix nitrogen and/or to survive nitrogen starvation. Furthermore, we use whole-genome sequence analysis of 58 Nostoc-resistant strains to identify several mutations associated with phage resistance, including in cell surface-related genes and regulatory genes involved in the development and function of heterocysts (cells specialized in nitrogen fixation). Finally, we employ phylogenetic analyses to show that most of these resistance genes are accessory genes whose evolution is impacted by lateral gene transfer events. Together, these results further our understanding of the interplay between diazotrophic Cyanobacteria and their phages and suggest that a tradeoff between phage resistance and nitrogen fixation affects the evolution of cell surface-related genes and of genes involved in heterocyst differentiation and nitrogen fixation.
(© The Author(s) 2024. Published by Oxford University Press on behalf of the International Society for Microbial Ecology.)

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Israel Water Authority; 1386/20 Israel Science Foundation

Keywords: Cyanobacteria; cost of resistance; genome evolution; nitrogen fixation; phage; resistance; tradeoff

N762921K75 (Nitrogen)

Date Created: 20240216 Date Completed: 20240219 Latest Revision: 20240219

20250114

PMC10811720

10.1093/ismejo/wrad008

38365231